NFAT5 represses canonical Wnt signaling via inhibition of β-catenin acetylation and participates in regulating intestinal cell differentiation

Cell Death and Disease

Volumn 4, Issue 6, 2013, Pages

  Wang, Q ^a,b   Zhou, Y ^a,b   Rychahou, P ^a,b   Liu, C ^a,b   Weiss, H L ^a,b,c   Evers, B M ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

catenin; intestinal cell differentiation; NFAT5; Wnt

Indexed keywords

ALKALINE PHOSPHATASE; BETA CATENIN; CALCINEURIN; HISTONE ACETYLTRANSFERASE PCAF; NFAT5 PROTEIN; SUCRASE; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ACETYLATION; ADULT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE CELL; INTESTINE MUCOSA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; WNT SIGNALING PATHWAY;

EID: 84879637463     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.202     Document Type: Article

References (47)

1. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. Am J Anat 1974; 141: 537-561.
2. Traber PG. Differentiation of intestinal epithelial cells: lessons from the study of intestinespecific gene expression. J Lab Clin Med 1994; 123: 467-477.
3. Muller MR, Rao A. NFAT, immunity and cancer: a transcription factor comes of age. Nat Rev Immunol 10: 645-656.
4. Hogan PG, Chen L, Nardone J, Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 2003; 17: 2205-2232.
5. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J et al. A calcineurindependent transcriptional pathway for cardiac hypertrophy. Cell 1998; 93: 215-228.
6. Yang TT, Xiong Q, Enslen H, Davis RJ, Chow CW. Phosphorylation of NFATc4 by p38 mitogen-activated protein kinases. Mol Cell Biol 2002; 22: 3892-3904.
7. Zhou Y, Wang Q, Guo Z, Weiss HL, Evers BM. Nuclear factor of activated T-cell c3 inhibition of mammalian target of rapamycin signaling through induction of regulated in development and DNA damage response 1 in human intestinal cells. Mol Biol Cell 23: 2963-2972.
8. Luo ML, Shen XM, Zhang Y, Wei F, Xu X, Cai Y et al. Amplification and overexpression of CTTN (EMS1) contribute to the metastasis of esophageal squamous cell carcinoma by promoting cell migration and anoikis resistance. Cancer Res 2006; 66: 11690-11699.
9. Santini MP, Talora C, Seki T, Bolgan L, Dotto GP. Cross talk among calcineurin, Sp1/Sp3, and NFAT in control of p21(WAF1/CIP1) expression in keratinocyte differentiation. Proc Natl Acad Sci USA 2001; 98: 9575-9580.
10. Kao SC, Wu H, Xie J, Chang CP, Ranish JA, Graef IA et al. Calcineurin/NFAT signaling is required for neuregulin-regulated Schwann cell differentiation. Science 2009; 323: 651-654.
11. Aramburu J, Drews-Elger K, Estrada-Gelonch A, Minguillon J, Morancho B, Santiago V et al. Regulation of the hypertonic stress response and other cellular functions by the Rel-like transcription factor NFAT5. Biochem Pharmacol 2006; 72: 1597-1604.
12. Pinto D, Gregorieff A, Begthel H, Clevers H. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev 2003; 17: 1709-1713.
13. Zhang W, Chen X, Kato Y, Evans PM, Yuan S, Yang J et al. Novel cross talk of Kruppel-like factor 4 and beta-catenin regulates normal intestinal homeostasis and tumor repression. Mol Cell Biol 2006; 26: 2055-2064.
14. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, Hatzis P et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 2005; 7: 381-386.
15. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 2004; 18: 1385-1390.
16. Eisenmann DM. Wnt signaling. In WormBook (ed.), The C. elegans Research Community WormBook, 2005. doi:10.1895/wormbook.1.7.1.
17. Saneyoshi T, Kume S, Amasaki Y, Mikoshiba K. The Wnt/calcium pathway activates NFAT and promotes ventral cell fate in Xenopus embryos. Nature 2002; 417: 295-299.
18. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW et al. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/-colon carcinoma. Science 1997; 275: 1784-1787.
19. Giles RH, van Es JH, Clevers H. Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta 2003; 1653: 1-24.
20. Hecht A, Vleminckx K, Stemmler MP, van Roy F, Kemler R. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J 2000; 19: 1839-1850.
21. Liu C, Kato Y, Zhang Z, Do VM, Yankner BA, He X. beta-Trcp couples beta-catenin phosphorylation-degradation and regulates Xenopus axis formation. Proc Natl Acad Sci USA 1999; 96: 6273-6278.
22. Levy L, Wei Y, Labalette C, Wu Y, Renard CA, Buendia MA et al. Acetylation of beta-catenin by p300 regulates beta-catenin-Tcf4 interaction. Mol Cell Biol 2004; 24: 3404-3414.
23. Evans PM, Chen X, Zhang W, Liu C. KLF4 interacts with beta-catenin/TCF4 and blocks p300/CBP recruitment by beta-catenin. Mol Cell Biol 30: 372-381.
24. Wang Q, Wang X, Hernandez A, Kim S, Evers BM. Inhibition of the phosphatidylinositol 3-kinase pathway contributes to HT29 and Caco-2 intestinal cell differentiation. Gastroenterology 2001; 120: 1381-1392.
25. Liu L, Luo Y, Chen L, Shen T, Xu B, Chen W et al. Rapamycin inhibits cytoskeleton reorganization and cell motility by suppressing RhoA expression and activity. J Biol Chem 285: 38362-38373.
26. Winer IS, Bommer GT, Gonik N, Fearon ER. Lysine residues Lys-19 and Lys-49 of beta-catenin regulate its levels and function in T cell factor transcriptional activation and neoplastic transformation. J Biol Chem 2006; 281: 26181-26187.
27. Daniels DL, Weis WI. ICAT inhibits beta-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol Cell 2002; 10: 573-584.
28. Huang T, Xie Z, Wang J, Li M, Jing N, Li L. Nuclear factor of activated T cells (NFAT) proteins repress canonical Wnt signaling via its interaction with Dishevelled (Dvl) protein and participate in regulating neural progenitor cell proliferation and differentiation. J Biol Chem 286: 37399-37405.
29. O'Connor RS, Mills ST, Jones KA, Ho SN, Pavlath GK. A combinatorial role for NFAT5 in both myoblast migration and differentiation during skeletal muscle myogenesis. J Cell Sci 2007; 120(Pt 1): 149-159.
30. Berga-Bolanos R, Drews-Elger K, Aramburu J, Lopez-Rodriguez C. NFAT5 regulates T lymphocyte homeostasis and CD24-dependent T cell expansion under pathologic hypernatremia. J Immunol 185: 6624-6635.
31. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002; 111: 241-250.
32. Go WY, Liu X, Roti MA, Liu F, Ho SN. NFAT5/TonEBP mutant mice define osmotic stress as a critical feature of the lymphoid microenvironment. Proc Natl Acad Sci USA 2004; 101: 10673-10678.
33. Drews-Elger K, Ortells MC, Rao A, Lopez-Rodriguez C, Aramburu J. The transcription factor NFAT5 is required for cyclin expression and cell cycle progression in cells exposed to hypertonic stress. PLoS One 2009; 4: e5245.
34. Halterman JA, Kwon HM, Wamhoff BR. Tonicity-independent regulation of the osmosensitive transcription factor TonEBP (NFAT5). Am J Physiol Cell Physiol 302: C1-C8.
35. Lopez-Rodriguez C, Antos CL, Shelton JM, Richardson JA, Lin F, Novobrantseva TI et al. Loss of NFAT5 results in renal atrophy and lack of tonicity-responsive gene expression. Proc Natl Acad Sci USA 2004; 101: 2392-2397.
36. Mak MC, Lam KM, Chan PK, Lau YB, Tang WH, Yeung PK et al. Embryonic lethality in mice lacking the nuclear factor of activated T cells 5 protein due to impaired cardiac development and function. PLoS One 6: e19186.
37. Wang Y, Ko BC, Yang JY, Lam TT, Jiang Z, Zhang J et al. Transgenic mice expressing dominant-negative osmotic-response element-binding protein (OREBP) in lens exhibit fiber cell elongation defect associated with increased DNA breaks. J Biol Chem 2005; 280: 19986-19991.
38. Yamamoto F, Yamamoto H. Effect of inhibition of glycogen synthase kinase-3 on cardiac hypertrophy during acute pressure overload. Gen Thorac Cardiovasc Surg 58: 263-264.
39. Gregory MA, Phang TL, Neviani P, Alvarez-Calderon F, Eide CA, O'Hare T et al. Wnt/Ca2\+/NFAT signaling maintains survival of Ph\+ leukemia cells upon inhibition of Bcr-Abl. Cancer Cell 18: 74-87.
40. Veeman MT, Axelrod JD, Moon RT. A second canon. Functions and mechanisms of betacatenin-independent Wnt signaling. Dev Cell 2003; 5: 367-377.
41. Adachi A, Takahashi T, Ogata T, Imoto-Tsubakimoto H, Nakanishi N, Ueyama T et al. NFAT5 regulates the canonical Wnt pathway and is required for cardiomyogenic differentiation. Biochem Biophys Res Commun 426: 317-323.
42. Zhang W, Yang J, Liu Y, Chen X, Yu T, Jia J et al. PR55 alpha, a regulatory subunit of PP2A, specifically regulates PP2A-mediated beta-catenin dephosphorylation. J Biol Chem 2009; 284: 22649-22656.
43. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall WS, Khvorova A. Rational siRNA design for RNA interference. Nat Biotechnol 2004; 22: 326-330.
44. Wang Q, Wang X, Evers BM. Induction of cIAP-2 in human colon cancer cells through PKC delta/NF-kappa B. J Biol Chem 2003; 278: 51091-51099.
45. Wang Q, Zhou Y, Wang X, Evers BM. Glycogen synthase kinase-3 is a negative regulator of extracellular signal-regulated kinase. Oncogene 2006; 25: 43-50.
46. Kim S, Domon-Dell C, Kang J, Chung DH, Freund JN, Evers BM. Down-regulation of the tumor suppressor PTEN by the tumor necrosis factor-alpha/nuclear factor-kappaB (NF-kappaB)-inducing kinase/NF-kappaB pathway is linked to a default IkappaB-alpha autoregulatory loop. J Biol Chem 2004; 279: 4285-4291.
47. Wang Q, Zhou Y, Wang X, Evers BM. p27 Kip1 nuclear localization and cyclin-dependent kinase inhibitory activity are regulated by glycogen synthase kinase-3 in human colon cancer cells. Cell Death Differ 2008; 15: 908-919.